Otoferlin deficiency in zebrafish results in defects in balance and hearing: Rescue of the balance and hearing phenotype with full-length and truncated forms of mouse otoferlin

Molecular and Cellular Biology

Volumn 35, Issue 6, 2015, Pages 1043-1054

  Chatterjee, Paroma ^a   Padmanarayana, Murugesh ^a   Abdullah, Nazish ^a   Holman, Chelsea L ^a   LaDu, Jane ^a   Tanguay, Robert L ^a   Johnson, Colin P ^a  

^a OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; MORPHOLINE; OTOFERLIN; UNCLASSIFIED DRUG;

ADULT; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BALANCE DISORDER; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GENE SILENCING; HAIR CELL; HAIR GROWTH; HEARING IMPAIRMENT; HUMAN; IMMUNOFLUORESCENCE MICROSCOPY; LOCOMOTION; MESENCEPHALON; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; RAT; ZEBRA FISH; ANIMAL; COCHLEAR HAIR CELL; COMPARATIVE STUDY; EXOCYTOSIS; HEARING; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SYNAPSE;

DANIO RERIO; VERTEBRATA;

ANIMALS; DEAFNESS; EXOCYTOSIS; HAIR CELLS, AUDITORY; HEARING; HUMANS; LOCOMOTION; MEMBRANE PROTEINS; MESENCEPHALON; MICE; PHENOTYPE; PROTEIN STRUCTURE, TERTIARY; SYNAPSES; ZEBRAFISH;

EID: 84923135747     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01439-14     Document Type: Article

References (56)

1. LeMasurier M, Gillespie PG. 2005. Hair-cell mechanotransduction and cochlear amplification. Neuron 48:403-415. http://dx.doi.org/10.1016/j.neuron.2005.10.017.
2. Nouvian R, Beutner D, Parsons TD, Moser T. 2006. Structure and function of the hair cell ribbon synapse. J Membr Biol 209:153-165. http://dx.doi.org/10.1007/s00232-005-0854-4.
3. Fuchs PA. 2005. Time and intensity coding at the hair cell's ribbon synapse. J Physiol 566:7-12. http://dx.doi.org/10.1113/jphysiol.2004.082214.
4. Khimich D, Nouvian R, Pujol R, Tom Dieck S, Egner A, Gundelfinger ED, Moser T. 2005. Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 434:889-894. http://dx.doi.org/10.1038/nature03418.
5. He S, Yang J. 2011. Maturation of neurotransmission in the developing rat cochlea: immunohistochemical evidence from differential expression of synaptophysin and synaptobrevin 2. Eur J Histochem 55(1):e2. http://dx.doi.org/10.4081/ejh.2011.e2.
6. McMahon HT, Missler M, Li C, Sudhof TC. 1995. Complexins-cytosolic proteins that regulate snap receptor function. Cell 83:111-119. http://dx.doi.org/10.1016/0092-8674(95)90239-2.
7. Reim K, Mansour M, Varoqueaux F, McMahon HT, Sudhof TC, Brose N, Rosenmund C. 2001. Complexins regulate a late step in Ca2+-dependent neurotransmitter release. Cell 104:71-81. http://dx.doi.org/10.1016/S0092-8674(01)00192-1.
8. Reim K, Wegmeyer H, Brandstatter JH, Xue MS, Rosenmund C, Dresbach T, Hofmann K, Brose N. 2005. Structurally and functionally unique complexins at retinal ribbon synapses. J Cell Biol 169:669-680. http://dx.doi.org/10.1083/jcb.200502115.
9. Strenzke N, Chanda S, Kopp-Scheinpflug C, Khimich D, Reim K, Bulankina AV, Neef A, Wolf F, Brose N, Xu-Friedman MA, Moser T. 2009. Complexin-I is required for high-fidelity transmission at the endbulb of held auditory synapse. J Neurosci 29:7991-8004. http://dx.doi.org/10.1523/JNEUROSCI.0632-09.2009.
10. Uthaiah RC, Hudspeth AJ. 2010. Molecular anatomy of the hair cell's ribbon synapse. J Neurosci 30:12387-12399. http://dx.doi.org/10.1523/JNEUROSCI.1014-10.2010.
11. Beurg M, Michalski N, Safieddine S, Bouleau Y, Schneggenburger R, Chapman ER, Petit C, Dulon D. 2010. Control of exocytosis by synaptotagmins and otoferlin in auditory hair cells. J Neurosci 30:13281-13290. http://dx.doi.org/10.1523/JNEUROSCI.2528-10.2010.
12. Johnson CP, Chapman ER. 2010. Otoferlin is a calcium sensor that directly regulates SNARE-mediated membrane fusion. J Cell Biol 191:187-197. http://dx.doi.org/10.1083/jcb.201002089.
13. Roux I, Safieddine S, Nouvian R, Grati M, Simmler MC, Bahloul A, Perfettini I, Le Gall M, Rostaing P, Hamard G, Triller A, Avan P, Moser T, Petit C. 2006. Otoferlin, defective in a human deafness form, is essential for exocytosis at the auditory ribbon synapse. Cell 127:277-289. http://dx.doi.org/10.1016/j.cell.2006.08.040.
14. Schug N, Braig C, Zimmermann U, Engel J, Winter H, Ruth P, Blin N, Pfister M, Kalbacher H, Knipper M. 2006. Differential expression of otoferlin in brain, vestibular system, immature and mature cochlea of the rat. Eur J Neurosci 24:3372-3380. http://dx.doi.org/10.1111/j.1460-9568.2006.05225.x.
15. Valiyaveettil M, Alamneh Y, Miller SA, Hammamieh R, Wang Y, Arun P, Wei Y, Oguntayo S, Nambiar MP. 2012. Preliminary studies on differential expression of auditory functional genes in the brain after repeated blast exposures. J Rehabil Res Dev 49:1153-1162. http://dx.doi.org/10.1682/JRRD.2011.09.0182.
16. Zak M, Bress A, Brandt N, Franz C, Ruth P, Pfister M, Knipper M, Blin N. 2012. Ergic2, a brain specific interacting partner of Otoferlin. Cell Physiol Biochem 29:941-948. http://dx.doi.org/10.1159/000188338.
17. Rodríguez-Ballesteros M, Reynoso R, Olarte M, Villamar M, Morera C, Santarelli R, Arslan E, Meda C, Curet C, Volter C, Sainz-Quevedo M, Castorina P, Ambrosetti U, Berrettini S, Frei K, Tedin S, Smith J, Cruz Tapia M, Cavalle L, Gelvez N, Primignani P, Gomez-Rosas E, Martin M, Moreno-Pelayo MA, Tamayo M, Moreno-Barral J, Moreno F, del Castillo I. 2008. A multicenter study on the prevalence and spectrum of mutations in the otoferlin gene (OTOF) in subjects with nonsyndromic hearing impairment and auditory neuropathy. Hum Mutat 29:823-831. http://dx.doi.org/10.1002/humu.20708.
18. Yasunaga S, Grati M, Cohen-Salmon M, El-Amraoui A, Mustapha M, Salem N, El-Zir E, Loiselet J, Petit C. 1999. A mutation in OTOF, encoding otoferlin, a FER-1-like protein, causes DFNB9, a nonsyndromic form of deafness. Nat Genet 21:363-369. http://dx.doi.org/10.1038/7693.
19. Marty NJ, Holman CL, Abdullah N, Johnson CP. 2013. The C2 domains of otoferlin, dysferlin, and myoferlin alter the packing of lipid bilayers. Biochemistry 52:5585-5592. http://dx.doi.org/10.1021/bi400432f.
20. Duncker SV, Franz C, Kuhn S, Schulte U, Campanelli D, Brandt N, Hirt B, Fakler B, Blin N, Ruth P, Engel J, Marcotti W, Zimmermann U, Knipper M. 2013. Otoferlin couples to clathrin-mediated endocytosis in mature cochlear inner hair cells. J Neurosci 33:9508-9519. http://dx.doi.org/10.1523/JNEUROSCI.5689-12.2013.
21. Heidrych P, Zimmermann U, Kuhn S, Franz C, Engel J, Duncker SV, Hirt B, Pusch CM, Ruth P, Pfister M, Marcotti W, Blin N, Knipper M. 2009. Otoferlin interacts with myosin VI: implications for maintenance of the basolateral synaptic structure of the inner hair cell. Hum Mol Genet 18:2779-2790. http://dx.doi.org/10.1093/hmg/ddp213.
22. Ramakrishnan NA, Drescher MJ, Drescher DG. 2009. Direct interaction of otoferlin with syntaxin 1A, SNAP-25, and the L-type voltage-gated calcium channel Cav13. J Biol Chem 284:1364-1372.
23. Ramakrishnan NA, Drescher MJ, Morley BJ, Kelley PM, Drescher DG. 2014. Calcium regulates molecular interactions of otoferlin with SNARE proteins required for hair cell exocytosis. J Biol Chem 289:8750-8766. http://dx.doi.org/10.1074/jbc.M113.480533.
24. Dulon D, Safieddine S, Jones SM, Petit C. 2009. Otoferlin is critical for a highly sensitive and linear calcium-dependent exocytosis at vestibular hair cell ribbon synapses. J Neurosci 29:10474-10487. http://dx.doi.org/10.1523/JNEUROSCI.1009-09.2009.
25. Schwander M, Sczaniecka A, Grillet N, Bailey JS, Avenarius M, Najmabadi H, Steffy BM, Federe GC, Lagler EA, Banan R, Hice R, Grabowski-Boase L, Keithley EM, Ryan AF, Housley GD, Wiltshire T, Smith RJH, Tarantino LM, Muller U. 2007. A forward genetics screen in mice identifies recessive deafness traits and reveals that pejvakin is essential for outer hair cell function. J Neurosci 27:2163-2175. http://dx.doi.org/10.1523/JNEUROSCI.4975-06.2007.
26. Vincent PF, Bouleau Y, Safieddine S, Petit C, Dulon D. 2014. Exocytotic machineries of vestibular type I and cochlear ribbon synapses display similar intrinsic otoferlin-dependent Ca2+ sensitivity but a different coupling to Ca2+ channels. J Neurosci 34:10853-10869. http://dx.doi.org/10.1523/JNEUROSCI.0947-14.2014.
27. Reisinger E, Bresee C, Neef J, Nair R, Reuter K, Bulankina A, Nouvian R, Koch M, Buckers J, Kastrup L, Roux I, Petit C, Hell SW, Brose N, Rhee JS, Kugler S, Brigande JV, Moser T. 2011. Probing the functional equivalence of otoferlin and synaptotagmin 1 in exocytosis. J Neurosci 31:4886-4895. http://dx.doi.org/10.1523/JNEUROSCI.5122-10.2011.
28. Leibovici M, Safieddine S, Petit C. 2008. Mouse models for human hereditary deafness. Curr Top Dev Biol 84:385-429. http://dx.doi.org/10.1016/S0070-2153(08)00608-X.
29. Westerfield M. 2000. The zebrafish book. A guide for the laboratory use of zebrafish (Danio rerio), 4th ed. University of Oregon Press, Eugene, OR.
30. Thisse C, Thisse B. 2008. High-resolution in situ hybridization to wholemount zebrafish embryos. Nat Protoc 3:59-69. http://dx.doi.org/10.1038/nprot.2007.514.
31. Novak AE, Ribera AB. 2003. Immunocytochemistry as a tool for zebrafish developmental neurobiology. Methods Cell Sci 25:79-83. http://dx.doi.org/10.1023/B:MICS.0000006894.43940.b1.
32. Sabaliauskas NA, Foutz CA, Mest JR, Budgeon LR, Sidor AT, Gershenson JA, Joshi SB, Cheng KC. 2006. High-throughput zebrafish histology. Methods 39:246-254. http://dx.doi.org/10.1016/j.ymeth.2006.03.001.
33. Javelle M, Marco CF, Timmermans M. 2011. In situ hybridization for the precise localization of transcripts in plants. J Vis Exp 2011(57):e3328. http://dx.doi.org/10.3791/3328.
34. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. 1995. Stages of embryonic development of the zebrafish. Dev Dyn 203:253-310. http://dx.doi.org/10.1002/aja.1002030302.
35. Waterman RE, Bell DH. 1984. Epithelial fusion during early semicircular canal formation in the embryonic zebrafish, Brachydanio rerio. Anat Rec 210:101-114. http://dx.doi.org/10.1002/ar.1092100113.
36. Goodyear RJ, Legan PK, Christiansen JR, Xia B, Korchagina J, Gale JE, Warchol ME, Corwin JT, Richardson GP. 2010. Identification of the hair cell soma-1 antigen, HCS-1, as otoferlin. J Assoc Res Otolaryngol 11:573-586. http://dx.doi.org/10.1007/s10162-010-0231-6.
37. Pangrsic T, Lasarow L, Reuter K, Takago H, Schwander M, Riedel D, Frank T, Tarantino LM, Bailey JS, Strenzke N, Brose N, Muller U, Reisinger E, Moser T. 2010. Hearing requires otoferlin-dependent efficient replenishment of synaptic vesicles in hair cells. Nat Neurosci 13:869-876. http://dx.doi.org/10.1038/nn.2578.
38. Griesinger CB, Richards CD, Ashmore JF. 2002. Fm1-43 reveals membrane recycling in adult inner hair cells of the mammalian cochlea. J Neurosci 22:3939-3952.
39. Kappler JA, Starr CJ, Chan DK, Kollmar R, Hudspeth AJ. 2004. A nonsense mutation in the gene encoding a zebrafish myosin VI isoform causes defects in hair-cell mechanotransduction. Proc Natl Acad Sci U S A 101:13056-13061. http://dx.doi.org/10.1073/pnas.0405224101.
40. Roux I, Hosie S, Johnson SL, Bahloul A, Cayet N, Nouaille S, Kros CJ, Petit C, Safieddine S. 2009. Myosin VI is required for the proper maturation and function of inner hair cell ribbon synapses. Hum Mol Genet 18:4615-4628. http://dx.doi.org/10.1093/hmg/ddp429.
41. Nicolson T, Rusch A, Friedrich RW, Granato M, Ruppersberg JP, Nusslein-Volhard C. 1998. Genetic analysis of vertebrate sensory hair cell mechanosensation: the zebrafish circler mutants. Neuron 20:271-283. http://dx.doi.org/10.1016/S0896-6273(00)80455-9.
42. Obholzer N, Wolfson S, Trapani JG, Mo W, Nechiporuk A, Busch-Nentwich E, Seiler C, Sidi S, Sollner C, Duncan RN, Boehland A, Nicolson T. 2008. Vesicular glutamate transporter 3 is required for synaptic transmission in zebrafish hair cells. J Neurosci 28:2110-2118. http://dx.doi.org/10.1523/JNEUROSCI.5230-07.2008.
43. Winata CL, Korzh S, Kondrychyn I, Zheng W, Korzh V, Gong Z. 2009. Development of zebrafish swimbladder: the requirement of Hedgehog signaling in specification and organization of the three tissue layers. Dev Biol 331:222-236. http://dx.doi.org/10.1016/j.ydbio.2009.04.035.
44. Khan Z, Carey J, Park HJ, Lehar M, Lasker D, Jinnah HA. 2004. Abnormal motor behavior and vestibular dysfunction in the stargazer mouse mutant. Neuroscience 127:785-796. http://dx.doi.org/10.1016/j.neuroscience.2004.05.052.
45. Lindema S, Gernet M, Bennay M, Koch M, Loscher W. 2008. Comparative analysis of anxiety-like behaviors and sensorimotor functions in two rat mutants, ci2 and ci3, with lateralized rotational behavior. Physiol Behav 93:417-426. http://dx.doi.org/10.1016/j.physbeh.2007.11.034.
46. Burgess HA, Granato M. 2007. Sensorimotor gating in larval zebrafish. J Neurosci 27:4984-4994. http://dx.doi.org/10.1523/JNEUROSCI.0615-07.2007.
47. Faber DS, Fetcho JR, Korn H. 1989. Neuronal networks underlying the escape response in goldfish. General implications for motor control. Ann N Y Acad Sci 563:11-33.
48. Zottoli SJ, Faber DS. 2000. The Mauthner cell: what has it taught us? Neuroscientist 6:26-38. http://dx.doi.org/10.1177/107385840000600111.
49. Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, Collins JE, Humphray S, McLaren K, Matthews L, McLaren S, Sealy I, Caccamo M, Churcher C, Scott C, Barrett JC, Koch R, Rauch GJ, White S, Chow W, Kilian B, Quintais LT, Guerra-Assuncao JA, Zhou Y, Gu Y, Yen J, Vogel JH, Eyre T, Redmond S, Banerjee R, Chi J, Fu B, Langley E, Maguire SF, Laird GK, Lloyd D, Kenyon E, Donaldson S, Sehra H, Almeida-King J, Loveland J, Trevanion S, Jones M, Quail M, Willey D, Hunt A, Burton J, Sims S, McLay K, Plumb B, Davis J, Clee C, Oliver K, Clark R, Riddle C, Elliot D, Threadgold G, Harden G, Ware D, Mortimore B, Kerry G, Heath P, Phillimore B, Tracey A, Corby N, Dunn M, Johnson C, Wood J, Clark S, Pelan S, Griffiths G, Smith M, Glithero R, Howden P, Barker N, Stevens C, Harley J, Holt K, Panagiotidis G, Lovell J, Beasley H, Henderson C, Gordon D, Auger K, Wright D, Collins J, Raisen C, Dyer L, Leung K, Robertson L, Ambridge K, Leongamornlert D, McGuire S, Gilderthorp R, Griffiths C, Manthravadi D, Nichol S, Barker G, Whitehead S, Kay M, Brown J, Murnane C, Gray E, Humphries M, Sycamore N, Barker D, Saunders D, Wallis J, Babbage A, Hammond S, Mashreghi-Mohammadi M, Barr L, Martin S, Wray P, Ellington A, Matthews N, Ellwood M, Woodmansey R, Clark G, Cooper J, Tromans A, Grafham D, Skuce C, Pandian R, Andrews R, Harrison E, Kimberley A, Garnett J, Fosker N, Hall R, Garner P, Kelly D, Bird C, Palmer S, Gehring I, Berger A, Dooley CM, Ersan-Urun Z, Eser C, Geiger H, Geisler M, Karotki L, Kirn A, Konantz J, Konantz M, Oberlander M, Rudolph-Geiger S, Teucke M, Osoegawa K, Zhu B, Rapp A, Widaa S, Langford C, Yang F, Carter NP, Harrow J, Ning Z, Herrero J, Searle SM, Enright A, Geisler R, Plasterk RH, Lee C, Westerfield M, de Jong PJ, Zon LI, Postlethwait JH, Nusslein-Volhard C, Hubbard TJ, Roest Crollius H, Rogers J, Stemple DL, Begum S, Lloyd C, Lanz C, Raddatz G, Schuster SC. 2013. The zebrafish reference genome sequence and its relationship to the human genome. Nature 496:498-503. http://dx.doi.org/10.1038/nature12111.
50. Yasunaga S, Grati M, Chardenoux S, Smith TN, Friedman TB, Lalwani AK, Wilcox ER, Petit C. 2000. OTOF encodes multiple long and short isoforms: genetic evidence that the long ones underlie recessive deafness DFNB9. Am J Hum Genet 67:591-600. http://dx.doi.org/10.1086/303049.
51. Longo-Guess C, Gagnon LH, Bergstrom DE, Johnson KR. 2007. A missense mutation in the conserved C2B domain of otoferlin causes deafness in a new mouse model of DFNB9. Hear Res 234:21-28. http://dx.doi.org/10.1016/j.heares.2007.09.005.
52. Mirghomizadeh F, Pfister M, Apaydin F, Petit C, Kupka S, Pusch CM, Zenner HP, Blin N. 2002. Substitutions in the conserved C2C domain of otoferlin cause DFNB9, a form of nonsyndromic autosomal recessive deafness. Neurobiol Dis 10:157-164. http://dx.doi.org/10.1006/nbdi.2002.0488.
53. Helfmann S, Neumann P, Tittmann K, Moser T, Ficner R, Reisinger E. 2011. The crystal structure of the C(2)A domain of otoferlin reveals an unconventional top loop region. J Mol Biol 406:479-490. http://dx.doi.org/10.1016/j.jmb.2010.12.031.
54. Abdullah N, Padmanarayana M, Marty NJ, Johnson CP. 2014. Quantitation of the calcium and membrane binding properties of the C2 domains of dysferlin. Biophys J 106:382-389. http://dx.doi.org/10.1016/j.bpj.2013.11.4492.
55. Therrien C, Di Fulvio S, Pickles S, Sinnreich M. 2009. Characterization of lipid binding specificities of dysferlin C2 domains reveals novel interactions with phosphoinositides. Biochemistry 48:2377-2384. http://dx.doi.org/10.1021/bi802242r.
56. Wright S, Hwang Y, Oertel D. 24 September 2014. Synaptic transmission between end bulbs of held and bushy cells in the cochlear nucleus of mice with a mutation in otoferlin. J Neurophysiol http://dx.doi.org/10.1152/jn.00522.2014.